He joined the UW football staff in 1946.[5] The three seasons he served as head coach of the UW football team were controversial. His record of 10 wins, 18 losses, and 2 ties was identified as the second worst in Seattle's history in a 2006 article by Seattle Post-Intelligencer columnist Jim Moore.[7] The team was involved in a payoff scandal that led to NCAA sanctions for the school and the firing of Cherberg in February, 1956.[8]

In June, 1956 Cherberg announced his candidacy for the Democratic nomination for lieutenant governor.[9] Capitalizing on name recognition from his football career and the statewide contacts he'd developed as the head of the state's association of high school football coaches, he won the Democratic primary by defeating Howard S. Bargreen,[10] and the general election by defeating Republican Don McDermott.[11]

Cherberg was inaugurated as Washington's lieutenant governor on January 16, 1957, under fellow DemocratAlbert D. Rosellini. For his first 15 years in office, he also worked as an account executive at Seattle-area TV station KIRO to supplement his then-low lieutenant governor salary.[3]

Following his defeat in the mayoral campaign, he once again ran for lieutenant governor. He served continuously under Republican Governor Daniel J. Evans (1965–1977), Democrat Dixy Lee Ray (1977–1981), Republican John D. Spellman (1981–1985), and for the first term of Democrat Booth Gardner (1985–1989). In his last race, he won comfortably with 63% of the vote.[3] Cherberg stepped down in the 1988 race having served as lieutenant governor for nearly one third of Washington state's history at the time; at his death, he was the longest serving lieutenant governor in United States history.[6]

Cherberg lived in Seattle until his death from pneumonia at age 81 in 1992.[16] He was interred at Calvary Cemetery,[6] about a mile (1.6 km) northeast of the University of Washington campus. The John A. Cherberg Building, which houses Washington State Senate offices at the State Capitol campus, was renamed in his honor.[2]